**4. Field effects (1): synergistic effects**

degree of DNA damage is linearly reflected in the biological consequences. These statements mean that biological effects can be predicted by the effective dose. Although this approach is widely accepted and utilized for assessing the biological impacts of nuclear disasters, the approach entirely ignores other potential molecular pathways and dismisses the complexity of the biological and ecological responses to the various known and unknown materials that

In contrast to the conventional targeted effects, the last two decades have experienced a surge of *nontargeted effects* of ionizing radiation [51–56]. The nontargeted effects include bystander effects, genomic instability, adaptive responses, and other modes, and these nontargeted effects are likely caused by the reactive oxygen species produced by irradiation [51–56]. In this sense, the nontarget effects may be referred to as the indirect effects (note that in this chapter, nontargeted effects are classified into the same category as the direct effects as a matter of convenience to some extent). In terms of the nontargeted effects, it is important to remember that they are not readily predictable by doses, and many of them are latent. Therefore, the nontarget effects may not be detected in acute irradiation experiments, but they may manifest in the field. Furthermore, the field-laboratory paradox discussed above may have originated, at least partly, from the influence of the nontargeted effects in the field. In fact, the nontargeted effects, such as genomic instability, may have played significant roles in the observed

However, even the nontarget effects may not adequately explain the all effects that manifest in the field. For example, there could be possible nonradioactive by-products released from a reactor and naturally occurring nonradioactive materials that are "activated" by the radioactive materials released from a reactor. There may also be ecological interactions that could amplify small irradiation effects to larger levels throughout a food web. These possibilities may be potential sources of the *field effects* (or more precisely, *field-specific effects*), which would not be observed in controlled laboratory experiments that use an artificial source of radiation, such as 60Co and chemically pure 137Cs. However, these field-specific effects should not be confused with (or dismissed as) confounding factors because these field effects are elicited by the nuclear accident. Similarly, nontargeted effects do not have to be field-specific effects; nontargeted effects may be observed in controlled laboratory experiments that use an artificial radiation source and a simple biological system, such as a cell culture system. In other words, the nontargeted effects may be uncovered with conventional radiation biology, which investigates universal mechanisms of radiation effects, but the field-specific effects may be uncovered with *pollution biology*, which investigates the real-world phenomena; however, these two fields cannot be separated in a meaningful way in the case of nuclear accidents.

In this chapter, I refer to both the conventional targeted effects and the nontargeted effects as the "direct" effects (or "primary" effects) (**Figure 1**); however, in some literature, the nontargeted effects or one mode of the nontargeted effect are referred to as the indirect effects. It is understood that laboratory-based controlled irradiation experiments, irrespective of high or low doses, primarily examine the direct effects of ionizing radiation. In contrast, as mentioned above, other potential unconventional indirect effects of nuclear pollution are collectively called the field effects (**Figure 1**) [48, 57]. The field effects are often dependent on a biological

increase in butterfly morphological abnormalities in the fall of 2012 [9, 13].

are released from nuclear reactors.

54 New Trends in Nuclear Science

(including ecological) context.

The biological indirect effects are a collective expression of all biological effects of the nuclear accident excluding the effects of the direct radiation exposure. Because any wild biological system has diverse and complex relationships with biological and chemical species, there are numerous indirect pathways that can affect organisms. Below, the field effects are roughly categorized into three groups: synergistic effects, effects from particulate matters, and ecological effects (**Figure 2**).

Although trehalose alone may not be a significant stressor, this case illustrates an example of an unexpected synergistic interaction between toxic substances that were otherwise benign

Understanding Low-Dose Exposure and Field Effects to Resolve the Field-Laboratory Paradox…

http://dx.doi.org/10.5772/intechopen.79870

57

Second, what was released from the Fukushima nuclear reactors was a plume of materials that caused *particulate air pollution*; regardless of whether these particulates were radioactive, the released materials were dispersed as atmospheric aerosols [67, 68]. There is no question that atmospheric aerosols cause respiratory and cardiovascular diseases in humans [69–72]. Indeed, natural radon attaches to air dust, and when this dust is inhaled, it is believed to cause lung cancer [73]. There is no reason to believe that the particulate air pollution from the nuclear reactors was safe for butterflies or other wild organisms. However, to my knowledge,

It should be noted that the plume from the nuclear reactors contained two types of radioactive materials: soluble and insoluble forms. Soluble materials, such as a form of inorganic salt, are solubilized quickly in environmental water. Additionally, insoluble materials have been detected as spherical particles [74, 75], and they are attached on the surface of any material. At least some of these particles (i.e., particulate matter) may bind to nonradioactive common air dust [68, 69]. Based on the results of the internal exposure experiments in which field-collected polluted leaves were fed to butterfly larvae, the ingestion of particulate matter present on the surface of leaves may have caused digestive and immunological effects [9–12].

Third, when one examines the interactions of multiple species based on a food web or an ecological system as a whole, one may be able to discover radiation effects that would not be discovered by a single-species approach; consequently, observations like this may indicate important field effects. This may be called *the ecological effects*. A similar concept has recently been addressed in radioecology [76]; however, this topic is often discussed from the viewpoint of the bioaccumulation of radioactive materials or organic materials in high-order consumers.

The ecological system that the pale grass blue butterfly inhabits is relatively simple due to its monophagous nature [48]. Thus, this butterfly and its associated ecosystem may serve as a "model ecosystem" to investigate both the population dynamics and the environmental influences through the ecological food web after the Fukushima nuclear accident. It appears that in the case of the pale grass blue butterfly "model ecosystem," the quality of its host plant, *Oxalis corniculata*, is probably important and is determined by the quality of the soil and air. When soil is contaminated with radioactive materials and other pollutants, such as agrochemicals, the quality of the host-plant leaves decreases. Similarly, air pollutants (i.e., particulate matter) that cover the surface of leaves, whether radioactive or not, may change the physiological

Although bioaccumulation is important, it is based on a dosimetric viewpoint.

environmental chemicals.

**5. Field effects (2): particulate matter**

any discussion from this viewpoint is scarce.

**6. Field effects (3): ecological effects**

**Figure 2.** Four possible types of effects on the larvae of the pale grass blue butterfly (green bars). Molecular ionization is the direct (i.e., primary) effect, while the other three modes (synergistic stress, particulate matter, and plant chemicals) are biological indirect (i.e., secondary) field effects.

First, *synergistic effects* with other environmental factors, including climate conditions and chemical stressors, may exist in the wild. When an organism experiences stress from a single source, the stress may be managed relatively well; however, when stress is imposed by two different sources, the harmful effects may be synergistically enhanced beyond their individual actions. In laboratory conditions, the "climate" conditions are usually constant, and additional stressors are not usually provided; thus, synergy is often difficult to predict using conventional irradiation experiments alone. Logically, the synergistic effects of radiation exposure and other stressors have been an important topic in radiation biology [52, 53, 58–61]. However, in my opinion, such synergistic stress effects have not been fully appreciated in radiation biology. Importantly, synergistic stress effects are not limited to exposure to radiation. Here, I briefly discuss two examples that may be insightful for this line of discussion.

A discrepancy has been recognized between the laboratory and field results in phenotypic plasticity studies. In an authoritative textbook, Gilbert and Epel [62] stated the following: "Phenotypic plasticity means that animals in the wild may develop differently than those in the laboratory" and "This has important consequences when we apply knowledge gained in the laboratory to a field science such as conservation biology." One specific example provided in the textbook states that some frog tadpoles are up to 46 times more sensitive to pesticides in the presence of predators that release chemicals in the wild than they are in the laboratory [63, 64]. The conclusion stated that "ignoring the relevant ecology can cause incorrect estimates of a pesticide's lethality in nature" [63]. I believe that the same principle applies to radioactive materials from nuclear reactors.

Another insightful case was reported in the epidemic caused by the bacterium *Clostridium difficile* [65, 66]. For this bacterial epidemic outbreak to occur in North America and Europe, the widespread use of a food additive, trehalose, played a crucial role. Infected mice had higher mortality rates when fed food that contained trehalose [66]. Without the trehalose-rich environment that newly emerged in this century, the deadly endemic would not have occurred. Although trehalose alone may not be a significant stressor, this case illustrates an example of an unexpected synergistic interaction between toxic substances that were otherwise benign environmental chemicals.
